many ways to get happy: pollination modes of european ... · wasps) which deter attackers. e....

144 Orchid Digest, July, Aug., Sept. 2016

Many Ways to Get Happy: pollination Modes of european epipactis species

Jean Claessens and JaCques Kleynen

summaryThe European members of the orchid genus Epipac-

tis shows a great variety of pollination modes, ranging from allogamy (reproducing by cross-fertilization) to autogamy (pollination of a flower by its own pollen) and a mixture of both. In this article the structure of the flower, the adaptations to the pollinators, as well as the changes in the column structure that enable self-pollination are discussed.

IntroductionThe species of the genus Epipactis are not among the

flashiest orchids that draw the attention of enthusiasts, like the genus Ophrys or the tropical orchids. Yet they are a quite interesting group. They show remarkable adaptations to their pollinators and have also adapted their mode of pollination to environmental conditions. In this article, we will examine several species of the ge-nus Epipactis and discuss their pollination mechanisms.

Pollination Mechanism of allogamous species

For better understanding of the changes in the con-struction and pollination mode of the flowers we will take Epipactis helleborine, the Broad-leaved Helleborine, as an example (fig. 1). This is a European species that has colonized North America successfully: in Wiscon-sin, it is considered a weed! It was first found in the USA in 1879, after which its population expanded rap-idly. In Europe, it is widespread and frequent. It prefers moderately shaded places and can be found in a wide variety of habitats: woods, bushes but also, man-made environments like parks, lanes, sidewalks and cemeter-ies.

The flowers are rather inconspicuous, possessing typical drab wasp-colors of reddish brown and dull purple, as can also be found in the genus Scrophularia (figworts), which have typical wasp flowers too. The perianth segments, the sepals and petals, are wide open (fig. 2). The lip is divided in two parts, the outer part

Fig. 01: E. helleborine. Fig. 02: E. helleborine, flower showing the anther (A) with the pollinia (P), the viscidium (V)

and the two parts of the lip, the hypochile (H) and the epichile (E)

©J.

Kle

ynen

©J.

Kle

ynen

Orchid Digest, July, Aug., Sept. 2016 145

(epichile) and inner part (hypochile). The epichile is broader than long, heart-shaped with two bosses (a pro-tuberance or roundish excrescence) at the center. The hypochile, where the nectar is secreted, is bowl-shaped and reddish-brown on the inside. In warm weather, you can see the glistening nectar it contains. Immedi-ately above the hypochile is the horizontal column, a fusion of the stamen and stigma, topped by the yellow anther cap which contains the pollinia. At anthesis (the opening of the flowers), the anther cap opens and re-leases the two yellow pollinia. At this stage, they are already connected to the underlying viscidium, a glob-ular structure consisting of milky viscid fluid covered by a thin membrane (fig. 3). The viscidium is placed at the upper rim of the large, rectangular, concave stigma, covered with sticky stigmatic fluid. The pollinia fall onto the slightly hollowed top of the column, which forms a pollen bed. The pollinia cannot fall out of this pollen bed because they are already connected to the viscidium. The powdery pollen within the pollinia co-heres rather well because it is interconnected by viscid threads.

Fig. 03: E. helleborine, close-up showing the anther (A) containing the pollinia (P), the globular viscidium (V)

and the large stigma (S) underneath

Fig. 04: E. helleborine, wasp bends to reach the nectar.

The shape and placement of the viscidium, stigma and pollen bed are crucial, because they can determine the pollination mode, as we will demonstrate later. In the case of Epipactis helleborine, the viscidium has a double function: it ensures that the pollinia are glued to a visiting insect and at the same time it prevents the pollinia from sliding forward and contacting the stig-ma. The large pollen bed ensures that the pollinia are in place. Thus, even if the pollinium could lose some pollen fragments, they are unable to slide onto the un-derlying stigma.

After the insect visitor (almost exclusively a wasp) has landed on the flower’s labellum (epichile), the head is position forward towards the hypochile. In order to reach the nectar, the wasp has to bend over the edge at a steep angle before it can start licking the nectar (fig. 04). In doing so, it bumps its head against the protrud-ing viscidium. The delicate membrane ruptures and the pollinia become instantly cemented to the wasp’s head (fig. 5). This obviously bothers the wasp, because it often starts grooming and trying to get rid of the pol-len load. If it does this immediately, it can remove the pollinia because the glue of the viscidium has not yet hardened completely. This is demonstrated by their pollinia, which can be seen sticking to various parts of the plants. However, within a few seconds the glue hardens and then it is no longer possible to remove the pollinia. After collecting an orchid’s pollinia the wasp is not deterred from visiting more orchid flowers (fig. 6).

attraction of InsectsThe flowers of Epipactis helleborine are not showy and

conspicuous like some orchids, but this is made up for by several other mechanisms that enhance their appeal to their pollinating insects. The flowers were thought to be scentless, but recent investigations showed that the nectar contains several compounds that are attrac-tive to wasps (vanillin derivatives, benzene, octanal, nonanal, and decanal). The composition of the nectar is an important feature, because certain compounds can make it toxic or repellent to some visitors. Also mi-crobes present in the nectar can change the nectar sugar composition.

©J.

Cla

esse

ns

©J.

Cla

esse

ns


Some visiting wasps can give an impression of “sluggish,” intoxicated behavior: they stay on the same flower for a longer time and crawl from one flower to another, rather than flying from one to the next like they normally do. Sometimes they even fall from a flower onto the ground when crawling around (see the You-Tube video: Orchid pollination 7: Pollination of Epipac-tis helleborine by wasps part 2)

Some researchers have suggested that warm weath-er causes the nectar to start fermenting, thus produc-ing ethanol which intoxicates the wasps. Since they frequently visit rotting fruit containing large quantities of yeast, fungi and bacteria, they can transport them to the orchid where they contaminate the nectar while feeding. Indeed, small quantities of ethanol, produced by such micro-organisms have been found. Other re-searchers found narcotic substances in the nectar. The morphinian oxycodone in particular seems to play an important role in intoxicating visiting insects. It is, however, not yet clear which substances influence the visitors under which circumstances. The composi-tion of the nectar has varied in different investigations; some researchers found yeast species in the nectar, other studies did not but found mainly microbial com-munities instead, mostly of the family of Enterobacte-riaceae. Weather conditions probably play an important role in the process of intoxication because we mostly observed “drunken” wasps in warm weather. We have seen enough evidence to conclude there is a definite ef-fect on the wasps. The cause of this is not yet clear, but lies in the composition of the nectar and the amount of contamination.

The presence of these contaminants may be advanta-geous to the orchid, because the insects stay longer on the flower spikes and pollinate more flowers. However,

Fig. 05: Vespula germanica with pollinia of E. helleborine.

Fig. 06: E. helleborine, visiting wasp with pollinia sticking to its forehead.

Fig. 07: E. helleborine, wasp with a bunch of pollinia.

©J.

Kle

ynen

©J.

Cla

esse

ns

©J.

Cla

esse

ns

this means the percentage of geitonogamy (flowers that are pollinated with pollen from the same flower spike) is considerable. Geitonogamy is equal to autogamy, which could be adverse to the plant. Epipactis helleborine is self-compatible, so it produces seeds, although the seeds originating from geitonogamous pollination may be of poor quality. But that is compensated for by the very high fruit set, of 76% on average. The wasps creep from one flower to another and the glue from the vis-cidium is very effective, so wasps often carry a whole bunch of pollinia on their foreheads (fig. 7). Obviously this hinders them in reaching the nectar, but it is a good means of augmenting pollen deposition. Also, the load on their heads obliges the wasps to push hard to reach the nectar, and as a result the pollinia are forced into the stigmatic fluid, thus increasing the number of massulae (a coherent mass of pollen grains that are deposited on the stigma).

Epipactis helleborine has another means of luring visi-tors. The plant produces GLVs (Green Leaf Volatiles), chemical signaling substances that are normally pro-duced by plants that are under attack by herbivores like caterpillars. The GLVs attract predators of the herbi-vores (in the case of caterpillars they are Ichneumonid wasps) which deter attackers. E. helleborine produces these substances although there is no predator around. This kind of attraction is called chemical mimicry and is an adaptation that is supposed to attract wasps that have not yet visited the orchid. Guided by the (false) alarm signal, the wasp inspects the flower and finds an adequate food source. The wasps learn to associate the scent with the reward, thus the loyalty of the visitors is reinforced. The shaded habitat, the scent, and spe-cific colors make this orchid attractive to a quite spe-cific group of pollinators, of which the main species are


Vespula vulgaris, V. germanica, Dolichovespula sylvestris, and D. saxonica.

Epipactis purpurata attracts wasps in the same way. This species grows in heavily shaded woods with few other accompanying plants. The structure and function of the column is the same as in E. helleborine (fig. 8). It is frequently visited by wasps and is noted for the many cases of “drunk wasps” falling off the flowers (fig. 9 and 10, also see the YouTube video: Orchid pol-lination 2: “Drunk wasp” falls off Epipactis purpurata).

Epipactis atrorubens is a species that differs from the other allogamous species. It has wine-red flowers and a distinct vanilla-scent (fig. 11). The scent seems to be quite strong and thus an excellent means of attracting insects from afar. One researcher observed that insects were overcome if they stayed too long on the flowers; a bumblebee caged in a tube with a flower spike of E. atrorubens died within 15 minutes. The color deviates from the typical wasp colors, so one may expect to find a different pollinator spectrum. Indeed, the orchid is not visited by wasps but mainly by bumble bees (fig. 12) and sometimes honeybees instead. Caged flowers did not set seed, indicating this orchid relies entirely on the pollinators for its reproduction. Bumblebees are

Fig. 08: E. purpurata, flower.

Fig. 09: Wasp carrying many pollinia approaches E. purpurata.

Fig. 10: The large amount of pollinia makes it almost impossible for the wasp to reach the nectar of E. purpurata.

©J.

Cla

esse

ns

©J.

Cla

esse

ns©

J. C

laes

sens


Fig. 13: E. palustris.

15). In order to reach the nectar, the insect must then crawl forward. The hypochile, now less loaded, returns to its original position and pushes the insect against the viscidium (fig. 16). As a result, the pollinia are glued

excellent pollinators making very few, fast visits per plant, thus assuring a high degree of cross pollination. Because of the speed of their visits, they can pollinate many plants in a short time. Fruit set of E. atrorubens is high (on average 66 %).

Transitional speciesEpipactis palustris is the most exotic looking, species

(fig. 13). It has purplish-white, wide open flowers with a ruffled, hinged lip. The epichile is white with yellow-orange margins, which serve as pseudo-pollen, attract-ing potential pollinators. The small quantities of nectar secreted in this region act as a preliminary reward for visiting insects, luring them further into the flower. Pur-plish lines guide the insects towards the center, where the orange hypochile produces copious nectar (fig. 14).

As in E. helleborine, the lip consists of two parts, but in E. palustris it is hinged, making the outer part, the epichile, movable. The column is horizontal and has a large stigma. The pollinia are yellow, long and stick for-ward, reaching beyond the upper rim of the pollen bed in which they lie. As in E. helleborine, there is a globular viscidium.

Darwin studied E. palustris and developed the “springboard” hypothesis in which he described how even the weight of a fly landing on the lip is sufficient for the articulated lip, the epichile, to bend down (fig.

Fig. 11: E. atrorubens, flowers.

Fig. 12: Bombus lucorum, a regular pollinator of E. atrorubens.

©J.

Kle

ynen

©J.

Cla

esse

ns©

J. C

laes

sens


Fig. 14: E. palustris, lip with orange margins at the epichile and copious nectar secretion in the hypochile.

©J.

Cla

esse

ns

Fig. 15: The digger wasp Ectemnius lapidarius has landed on the lip of E. palustris. The epichile bends down under its weight.

Fig. 16: Ectemnius lapidarius creeps towards the nectar, the hinged epichile bends upwards

and pushes the hoverfly against the viscidium.

©J.

Cla

esse

ns

©J.

Cla

esse

ns


to the insect (fig. 17). Our observations showed that, at least in young flowers, small insects are indeed pushed upwards where they receive a pollen load. Larger in-sects like honey bees have to perform a kind of balanc-ing act, because the epichile bends down completely when they land (fig. 18). They are large enough to reach the nectar, so they do not need to bend forward. But because of the effort it takes to maintain their balance, there is a good chance they will touch the viscidium.

Epipactis palustris is well visited by insects, primarily by honey bees, solitary bees and hoverflies. In the liter-ature, we found a total of 142 different pollinators were mentioned. And yet, if the weather conditions are bad (too hot, cold, or rainy) this orchid can resort to self-pollination. The pollinia are more friable than those of

E. helleborine and can crumble at the end of anthesis if the flower is not pollinated. The pollen fragments can then fall onto the stigma, assuring autogamy and a high fruit set of on average 77%.

Climatic conditions also determine the pollination mode of another Epipactis species, E. helleborine ssp. neerlandica. This is a dune-form which normally de-pends on wasps for its pollination. But we observed a change of pollination mode in a hot and dry summer When the pollinia disintegrated and the fragments fell onto the stigma, just as in E. palustris. In extreme con-ditions in Denmark this species even becomes totally autogamous. These plants grow in dunes called “the Danish Sahara,” where a constant hard wind blows, shutting the door to all visitors, which would literally be “sandblasted.” Because of these environmental con-ditions and lack of pollinators this primarily alloga-mous species has changed its pollination strategy.

autogamous speciesOrchids that change from allogamy to autogamy do

not have to go through huge changes. Minor changes of the column are sufficient to alter the pollination mode. In order to enable autogamy, the pollen should be able to reach the stigma. This is achieved by various adapta-

Fig. 17: While licking the nectar, this solitary wasp pushes the pollinia into the stigmatic fluid.

Fig. 18: The epichile bends down under the weight of a visit-ing honeybee (Apis mellifera).

Fig. 19: Underside of the column of E. leptochila, showing a reduced pollen bed, a non functional viscidium and loose pollen grains that

have already contacted the stigma.

©J.

Cla

esse

ns

©J.

Cla

esse

ns©

J. C

laes

sens


Fig. 20: E. leptochila, an autogamous species. Fig. 21: E. muelleri, another autogamous species.

Caption: Fig. 22: Longitudinal section of a flower bud of E. muelleri, showing the reduced pollen bed (arrow) and the pollinia already

sticking onto the stigma.

©J.

Cla

esse

ns

©J.

Cla

esse

ns

©J.

Cla

esse

ns

tions of the column morphology. All autogamous spe-cies show a reduced pollen bed and a reduced upper stigmatic rim. Thus the large pollinia can easily contact the stigmatic fluid below. The pollinia also undergo a transformation: they lose coherence, becoming more friable, falling apart in pieces. Most autogamous spe-cies show a viscidium that is reduced or even com-pletely disappeared (fig. 19). These changes enable easy

contact between pollinia and stigma combined with a reduced chance of pollen transport by insects.

Epipactis leptochila (fig. 20) is an example of an orchid that still shows some allogamous features like nectar and scent production but is in general totally autoga-mous. It can even be cleistogamous, making insect vis-its impossible.

In Epipactis muelleri (fig. 21) the pollen bed has al-most completely disappeared. When the anther opens, the pollinia fall down onto the underlying stigma and stick to it like two little horns (fig. 22).

But then why should an orchid turn towards au-togamy, which is genetically seen as a dead end, be-cause there is no more gene exchange? The answer is that autogamy is a good way of conquering new niches in circumstances where there are few or no pollinators. The more extreme the conditions are in which an orchid grows, the higher the chance that it will turn towards autogamy. Many Epipactis species have penetrated into the deep shade of forests, because there was no need to attract pollinators. Autogamy is rarely absolute; there is always a chance that an insect loaded with pollen from an allogamous species might visit the autogamous spe-cies, assuring some gene transfer. Anthropogenic fac-tors (the destruction of the original habitats, leaving only small suitable patches for the orchids) probably also contributed to the switch of pollination mode.


The genus Epipactis is a great showcase to illustrate how the column structure has adapted to meet the re-quirements of a changing habitat. Interested? You can find more examples of the flower-pollinator relation-ship in our book “The Flower of the European Orchid – Form and Function.”^

acknowledgementsWe want to thank Irene Palmer for her great help in

improving the text.

ReferencesClaessens, Jean, and Jacques Kleynen. 2011. “The Flow-

er of The European Orchid - Form and Function.” Geulle: Jean Claessens & Jacques Kleynen.

Darwin, Charles. 1877. “The Various Contrivances by which British and Foreign Orchids are Fertilised by Insects.” 2nd ed. London: John Murray.

Jakubska, A, D Przado, M Steininger, J Aniol-Kwiat-kowska, and M Kadej. 2005. “Why do Pollinators Become Sluggish?” Nectar Chemical Constituents from Epipactis helleborine(L.) Crantz (Orchidaceae).” Applied Ecology and Environmental Research 3 (2):29-38.

Kolanowska, Marta. 2013. “Niche Conservatism and the Future Potential Range of Epipactis helleborine (Orchidaceae).” PloS one 8 (10): e77352.

Nilsson, L. Anders. 1981. “Pollination ecology and evo-lutionary processes in six species of orchids.” Vol. 593: Stockholm: Almqvist and Wiksell Internat. In: Acta Univ. Upsaliensis, Science.

Richards, A. J. 1982. The influence of minor structur-al changes in the flower on breeding systems and speciation in Epipactis Zinn (Orchidaceae). In: Arm-strong, J. A., Powell, J. M., Richards, A. J. ed (s). Pol-lination and evolution: Symposium on Pollination Bi-ology held during the 13th International Botanical Congress, Sydney.

Robatsch, K. 1983. Blütenbiologie und Autogamie der Gattung Epipactis. Jahresbericht des Naturwissen-schaftlichen Vereins in Wuppertal 36:25-32.

Wilcox, Y. 2015. Epipactis palustris (L.) Crantz 1769 et ses pollinisateurs en Vendée. L’Orchidophile 206: 253-281.

about the authorsJean Claessens and

Jacques Kleynen are both teachers. They have writ-ten many articles about European orchids. Their special interest is mac-rophotography and the relationship between

the form of an orchid flower and its pollinator. This resulted in the publication of a book: “The Flower of the European Orchid – Form and Function,” which was published in 2011. The authors have spoken at many meetings of orchid societies and at conferences. Their website is: www.europeanorchids.com Jean Claessense-mail: [email protected]

Jacques Kleynen e-mail: [email protected]

View publication statsView publication stats

https://www.researchgate.net/publication/305651980

many ways to get happy: pollination modes of european ... · wasps) which deter attackers. e....

Documents